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Selection of Connective Tissue Progenitors Based SELECTION OF CONNECTIVE TISSUE PROGENITORS BASED ON CELL-ASSOCIATED HYALURONAN FOR ENHANCED BONE REGENERATION By Tonya Caralla Submitted in partial fulfillment of the requirements for the degree of Doctor of Philosophy Department of Biomedical Engineering CASE WESTERN RESERVE UNIVERSITY August 2012 Case Western Reserve University School of Graduate Studies We hereby approve the dissertation of Tonya Caralla Candidate for the Doctor of Philosophy degree*. Committee Members: Steven Eppell, chair and academic advisor George Muschler, research advisor Horst von Recum Vincent Hascall Maciej Zborowski Defense date: November 4th, 2011 *We also certify that written approval has been obtained for any proprietary material contained therein. 1 Dedication: There have been many who have contributed to my growth; both as a researcher and a person. I would like to take a moment to acknowledge those who have shaped me into the person I am today – this dissertation is for you too. To God, for bestowing on my countless blessings, a loving family, supportive friends, an amazing husband, and a giant brain. To my father Louis Caralla, who has always pushed me to be the best and brightest version of myself, who pushed me toward engineering and graduate school, and who left this earth last year before he could see this doctorate completed. I held his hand as he passed away, and I hope he will be holding mine as I go through this dissertation defense. I love you Dad, and I miss you every day. To my mother Becky, who has always been there to nurture me and listen to me whine before telling me to suck it up. It‟s a fine line, and she‟s walked it well. Thank you for always telling me that I could do anything that I wanted, for tackling the unglamorous job of raising me (especially as a surly know-it-all teen), and for bestowing on me both Barbies and Legos. To my sister Alyssa, who was my creative outlet and fellow troublemaker as we grew up moving around the Midwest. Not just anyone would play Legos with me for hours and then cheerfully dig up the neighbor‟s yard together. I admire your brain for being the opposite of mine, your patience, and your self-confidence at literally everything you do. I still remember that you ruined my sticker collection though. 2 To my loving husband Joe, for being my rock through hard times and a constant source of joy and backrubs. I would not have gotten through the last 4 years without your love and support, and I am so excited to spend the rest of my life with you. To my friends, who have become my family in Cleves and who offer excellent advice and unconditional love. They are patient, fantastic listeners, and always there when I need them (whether or not they are actually there in person). Leslie, Jones, Sam, Jen, Brandy, Maria, Amanda, Aniq, Kanger – love you guys! To my co-workers at the CCF, who are a font of knowledge and are always willing to take time to help me think through experiments, especially Cynthia, Chris, Vivek, Viviane and Sandra. To my committee, especially my advisor Dr. Muschler, who have pushed me to think deeper and become a better scientist, engineer, and researcher. 3 Table of Contents: Committee Approval Sheet……………………………………………………………..1 Dedication……….………………………………………………………………………2 Contents ...........................................................................................................................4 List of Tables ..................................................................................................................10 List of Figures .................................................................................................................11 Abstract………………………………………………………………………………….13 Executive Summary…………………………………………………………………….15 Chapter 1 Introduction to the Bone Tissue Engineering Paradigm, Connective Tissue Progenitor Cells, and Hyaluronan...................................................................................21 1.1. Clinical need for bone grafts……………………………………………………...21 1.2. Bone tissue engineering paradigm………………………………………………..21 1.3. Materials used for bone grafts…………………………………………………....22 1.4. Need for osteogenic cells……………………………………………..……….…24 1.5 Osteogenic cells present in bone marrow………………………………………....26 1.6 Review of the properties of hyaluronan…………………………………………..28 1.6.1 Composition………………………………………………………………....…28 1.6.2. Size and physical properties………………………………………………....…29 1.6.3. Degradation………………………………………………………………….….30 1.7 HA configuration in vivo……………………………………………………..…...31 1.8 Hyaluronan in disease states: inflammation, wound healing, and angiogenesis …35 1.9 Hyaluronan in the bone marrow…………………………………………………..36 1.10 Concept of a stem cell niche……………………………………………………....37 1.11 Hematopoietic stem cell niche……………………………………………...……..37 1.12 Evidence for CTP niche……………………………………………………….…..39 1.13 References………………………………………………………………………....43 Chapter 2 Introduction to Cell Separation Methods and Cell Surface Marker Characterization of CTPs……………………………………...………………………...64 2.1 Use of autologous bone marrow in bone defects………………………………..…64 2.2 Density gradient separation methods for cell separation…………………………..65 2.3 Selective Retention methods for cell separation…………………………………...66 2.4 Fluorescence activated cell sorting (FACS) for cell separation ………………...…68 2.5 Magnetic separation technologies for cell separation……………………………...69 2.6 Magnetic Theory………………………………………………………………..….69 2.7 Types of Magnetism……………………………………………………………….71 2.8 Clinical Application of Magnetic Separation Systems………………………….…73 2.9 Advantages of commercially available magnetic separation systems……………..74 2.10 Geometry of the Magnet………………………………………………………...…76 2.11 Cell surface markers used to select CTPs……………………………………….…77 2.11.1 Selection based on STRO-1……………………………………………………81 2.11.1 Selection based on CD105…………………………………………………..…82 2.11.3 Separation based on CD49a……………………………………………………82 2.11.4 Separation based on CD73……………………………………………………..83 4 2.11.5 Selection based on CD271……………………………………………………..83 2.11.6 Separation based on CD146……………………………………………………84 2.12 References………………………………………………………………………….86 Chapter 3 Hyaluronan as a novel marker for rapid selection of connective tissue progenitors……………………………..…………………………………………...……….93 3.1 Abstract………………….…………………………………………………………93 3.2 Introduction……………………………………………………………………..…94 3.3 Methods……………………………………………………………………………96 3.3.1 Cell Sources……………………………………………………………………...96 3.3.2 Magnetic Separation……………………………………………………………..97 3.3.3 Hematopoietic Progenitor Cells (HPC) Assay…………………………………..98 3.3.4 Colony Forming Unit Assay for CTP-Os………………………………………..98 3.3.5 Image Analysis………………………………………………………………..…99 3.3.6 Flow Cytometry………………………………………………………………...100 3.3.7 Statistical Analysis……………………………………………………………...102 3.4 Results…………………………………………………………………………….102 3.4.1 Cell and CTP Yield……………………………………………………………..102 3.4.2 Purity and Recovery…………………………………………………………….104 3.4.3 Four color flow cytometric analysis……………………………………………106 3.4.4 Selection of Colony Forming HPCs……………………………………………107 3.4.5 Selection of Colony Forming CTPs……………………………………………109 3.4.6 Biological Performance of Colonies Derived form CTPs Isolated in the HA+++, HA+, and HA-…………………………………………………………………………...109 3.4.6.1 Proliferation…………………………………………………………….109 3.4.6.2 Alkaline Phosphatase Activity………………………………………….110 3.4.6.3 Retained versus Newly Synthesized Hyaluronan………………………112 3.5 Discussion ………………………………………………………………………..113 3.6 Acknowledgments………………………………………………………………..116 3.7 References………………………………………………………………………..116 Chapter 4: A Model of Retention of Magnetized Cells in the EasySep Magnetic Separation System………………………………………………………………….……………119 Abstract………………………………………………………………………………... 119 4.1 Introduction……………………………………………………………………….120 4.2 Materials and Methods…………………………………………..………………. 122 4.2.1 Magnetic Labeling in the EasySepTM System…………………….…………… 122 4.2.2 Geometry of the EasySep Magnet……………………….……………………. 123 4.2.3 Magnetic Flux Density of the EasySep Magnet….…….………..……………..124 4.2.4 Testing with standardized Micromod beads……………………..……………. 125 4.2.5 Generation of HA+++ cells for CTV analysis………………………..…………. 126 4.2.6 Cell Tracking Velocimetry………………….………………………………… 127 4.3 Theory and Calculations………………………………………………………... 128 4.3.1 Derivation of model…………………………………………………………... 128 4.3.2 Relating model equation to magnetophoretic mobility……………………….. 132 4.4 Results…………………………………………………………………………... 135 5 4.4.1 Standardized Micromod Beads……………………………………………….. 135 4.4.2 Cell Tracking Velocimetry (CTV)……………………………………………. 138 4.5 Discussion………………………………………………………………………. 142 4.6 Appendi…………………………………………………………………………. 144 4.6.1 Appendix A: Justification: Neglecting the Inertial Term…………………….. 144 4.6.2 Appendix B: Justification: Sedimentation << Magnetic Displacement……… 145 4.7 References………………………………………………………………………. 150 Chapter 5 Development of protocol for magnetic separation based on hyaluronan for enrichment of connective tissue progenitors……………………………………………152 5. Chapter Introduction…………………….…………………………………………152 5.1 Evaluation of a method for RBC removal: LymphoprepTM Separation………..…154 5.1.1 Introduction……………………………………………………………..………154 5.1.2 Methods…………………………………………………………………………156 5.1.2.1 Cell Source……………………………………………………………...156 5.1.2.2 Description of LymphoprepTM Protocols……………………………….156 5.1.2.3 Cell Culture Conditions………………………………………………...158 5.1.2.4 ColonyzeTM Image Acquisition and Analysis…………………………. 159 5.1.2.5 Statistical Analysis…………………………………………………….. 159 5.1.3 Results…………………………………………………………………………. 159 5.1.3.1
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